Ant symbioses: colony-level effects of antagonistic and mutualistic interactions in two model ant systems

Abstract

An ant colony can be considered a superorganism with the workers analogous to cells and the entire colony analogous to an organism. Few studies have taken a colony-level approach to understanding how ant societies function. This dissertation explores how ant colonies respond and adjust to changes in the environment brought about through symbiotic relationships. First, I focus on the antagonistic interaction between a specialized phorid fly parasitoid and its host, the red imported fire ant, Solenopsis invicta. Phorid flies, which inject their eggs into fire ant workers, have recently been introduced into the United States as a biological control agent of this invasive pest, but the impact of these flies on fire ant populations is yet unknown. I examine how phorids affect colony growth, foraging efficiency, and caste recruitment of S. invicta. This study is the first to link indirect (behavioral modification of foraging) and direct (mortality to workers) effects of parasitic flies on fire ants. Second, I focus on the mutualistic interaction between ant farmers and their cultivated fungi. An intriguing dimension of complexity in the attine ant-fungus mutualism derives from potential conflict over the sex ratio, i.e., the ratio of male to female reproductives produced by a social insect colony. In hymenopteran societies, conflict over sex ratios is presumed to exist between the mother queen and her daughters (workers) due to differences in their genetic relatedness to the sexuals. The presence of heterospecific symbionts in a social insect colony (e.g., fungus-growing ants) complicates predictions of conflict resolution even furthermore. Three parties are potentially in conflict over sex ratios: the mutualistic fungus, the workers, and the queen. I studied the dynamics of sex-ratio conflict and ant-fungus cooperation in the primitive attine, Cyphomyrmex muelleri. I show that ants and native cultivars have coevolved to enhance mutualistic interactions. Despite these cooperative interactions, ant-cultivar conflict may have been revealed by the effect of cultivar switches on ant sex ratio and male survival. In sum, this work demonstrates that the integration of colony-level and individual-level investigations provides a comprehensive understanding of how ant societies (superorganisms) function and respond to their symbiotic partners.